Table of Contents Author Guidelines Submit a Manuscript
Table of Contents Alerts

To receive news and publication updates for International Journal of Endocrinology, enter your email address in the box below.

International Journal of Endocrinology
Volume 2018, Article ID 3271948, 20 pages
https://doi.org/10.1155/2018/3271948
Review Article

Melatonin: An Anti-Tumor Agent in Hormone-Dependent Cancers

Javier Menéndez-Menéndez and Carlos Martínez-Campa

Department of Physiology and Pharmacology, School of Medicine, University of Cantabria and Instituto de Investigación Valdecilla (IDIVAL), 39011 Santander, Spain

Correspondence should be addressed to Carlos Martínez-Campa; se.nacinu@mczenitram

Received 11 June 2018; Revised 30 July 2018; Accepted 12 August 2018; Published 2 October 2018

Academic Editor: Dario Acuña-Castroviejo

Copyright © 2018 Javier Menéndez-Menéndez and Carlos Martínez-Campa. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. A. B. Lerner, J. D. Case, Y. Takahashi, T. H. Lee, and W. Mori, “Isolation of melatonin, the pineal gland factor that lightens melanocytes,” Journal of the American Chemical Society, vol. 80, no. 10, pp. 2587–2587, 1958. View at Publisher · View at Google Scholar · View at Scopus
  2. R. J. Reiter, “Pineal melatonin: cell biology of its synthesis and of its physiological interactions,” Endocrine Reviews, vol. 12, no. 2, pp. 151–180, 1991. View at Publisher · View at Google Scholar · View at Scopus
  3. R. J. Reiter, J. C. Mayo, D. X. Tan, R. M. Sainz, M. Alatorre-Jimenez, and L. Qin, “Melatonin as an antioxidant: under promises but over delivers,” Journal of Pineal Research, vol. 61, no. 3, pp. 253–278, 2016. View at Publisher · View at Google Scholar · View at Scopus
  4. Z. Zhang, P. F. Inserra, B. Liang et al., “Melatonin, immune modulation and aging,” Autoimmunity, vol. 26, no. 1, pp. 43–53, 1997. View at Publisher · View at Google Scholar · View at Scopus
  5. N. Zisapel, “New perspectives on the role of melatonin in human sleep, circadian rhythms and their regulation,” British Journal of Pharmacology, vol. 175, no. 16, pp. 3190–3199, 2018. View at Publisher · View at Google Scholar · View at Scopus
  6. C. Martínez-Campa, J. Menéndez-Menéndez, C. Alonso-González, A. González, V. Álvarez-García, and S. Cos, “What is known about melatonin, chemotherapy and altered gene expression in breast cancer,” Oncology Letters, vol. 13, no. 4, pp. 2003–2014, 2017. View at Publisher · View at Google Scholar · View at Scopus
  7. D. E. Blask, L. A. Sauer, and R. T. Dauchy, “Melatonin as a chronobiotic/anticancer agent: cellular, biochemical and molecular mechanisms of action and their implications for circadian-based cancer therapy,” Current Topics in Medicinal Chemistry, vol. 2, no. 2, pp. 113–132, 2002. View at Publisher · View at Google Scholar · View at Scopus
  8. R. J. Reiter, S. A. Rosales-Corral, D. Acuna-Castroviejo, L. Qin, S.-F. Yang, and K. Xu, “Melatonin, a full service anti-cancer agent: inhibition of initiation, progression and metastasis,” International Journal of Molecular Sciences, vol. 18, no. 4, 2017. View at Publisher · View at Google Scholar · View at Scopus
  9. M. D. Mediavilla, E. J. Sanchez-Barcelo, D. X. Tan, L. Manchester, and R. J. Reiter, “Basic mechanisms involved in the anti-cancer effects of melatonin,” Current Medicinal Chemistry, vol. 17, no. 36, pp. 4462–4481, 2010. View at Publisher · View at Google Scholar · View at Scopus
  10. American Cancer Society, “Cancer Facts and Figures,” 2017, May 2018, http://www.cancer.org/research/cancer-facts-statistics/all-cancer-facts-figures/cancer-facts-figures-2017.html. View at Google Scholar
  11. C. T. Beatson, “On the treatment of inoperable cases of carcinoma of the mamma: suggestions for a new method of treatment with illustrative cases,” The Lancet, vol. 148, no. 3803, pp. 162–165, 1896. View at Publisher · View at Google Scholar · View at Scopus
  12. I. H. Russo and J. Russo, “Role of hormones in mammary cancer initiation and progression,” Journal of Pineal Research, vol. 3, no. 1, pp. 49–61, 1998. View at Publisher · View at Google Scholar · View at Scopus
  13. M. Cohen, M. Lippman, and B. Chabner, “Role of pineal gland in aetiology and treatment of breast cancer,” The Lancet, vol. 312, no. 8094, pp. 814–816, 1978. View at Publisher · View at Google Scholar · View at Scopus
  14. L. Tamarkin, D. Danforth, A. Lichter et al., “Decreased nocturnal plasma melatonin peak in patients with estrogen receptor positive breast cancer,” Science, vol. 216, no. 4549, pp. 1003–1005, 1982. View at Publisher · View at Google Scholar · View at Scopus
  15. R. G. Stevens, “Electric power use and breast cancer: a hypothesis,” American Journal of Epidemiology, vol. 125, no. 4, pp. 556–561, 1987. View at Publisher · View at Google Scholar · View at Scopus
  16. E. S. Schernhammer, F. Laden, F. E. Speizer et al., “Rotating night shifts and risk of breast cancer in women participating in the nurses’ health study,” Journal of the National Cancer Institute, vol. 93, no. 20, pp. 1563–1568, 2001. View at Publisher · View at Google Scholar · View at Scopus
  17. P. James, K. A. Bertrand, J. E. Hart, E. S. Schernhammer, R. M. Tamimi, and F. Laden, “Outdoor light at night and breast cancer incidence in the nurses’ health study II,” Environmental Health Perspectives, vol. 125, no. 8, article 087010, 2017. View at Publisher · View at Google Scholar · View at Scopus
  18. A. Garcia-Saenz, A. Sánchez de Miguel, A. Espinosa et al., “Evaluating the association between artificial light-at-night exposure and breast and prostate cancer risk in Spain (MCC-Spain study),” Environmental Health Perspectives, vol. 126, no. 4, article 047011, 2018. View at Publisher · View at Google Scholar · View at Scopus
  19. L. S. Kothari, P. N. Shah, and M. C. Mhatre, “Pineal ablation in varying photoperiods and the incidence of 9,10-dimethyl-1,2-benzanthracene induced mammary cancer in rats,” Cancer Letters, vol. 22, no. 1, pp. 99–102, 1984. View at Publisher · View at Google Scholar · View at Scopus
  20. D. E. Blask, D. B. Pelletier, S. M. Hill et al., “Pineal melatonin inhibition of tumor promotion in the N-nitroso-N-methylurea model of mammary carcinogenesis: potential involvement of antiestrogenic mechanisms in vivo,” Journal of Cancer Research and Clinical Oncology, vol. 117, no. 6, pp. 526–532, 1991. View at Publisher · View at Google Scholar · View at Scopus
  21. A. Gonzalez, S. Cos, C. Martinez-Campa et al., “Selective estrogen enzyme modulator actions of melatonin in human breast cancer cells,” Journal of Pineal Research, vol. 45, no. 1, pp. 86–92, 2008. View at Publisher · View at Google Scholar · View at Scopus
  22. S. Cos, A. González, C. Martínez-Campa, M. D. Mediavilla, C. Alonso-González, and E. J. Sánchez-Barceló, “Estrogen-signaling pathway: a link between breast cancer and melatonin oncostatic actions,” Cancer Detection and Prevention, vol. 30, no. 2, pp. 118–128, 2006. View at Publisher · View at Google Scholar · View at Scopus
  23. A. K. Shiau, D. Barstad, P. M. Loria et al., “The structural basis of estrogen receptor/coactivator recognition and the antagonism of this interaction by tamoxifen,” Cell, vol. 95, no. 7, pp. 927–937, 1998. View at Publisher · View at Google Scholar · View at Scopus
  24. T. M. Molis, L. L. Spriggs, and S. M. Hill, “Modulation of estrogen receptor mRNA expression by melatonin in MCF-7 human breast cancer cells,” Molecular Endocrinology, vol. 8, no. 12, pp. 1681–1690, 1994. View at Publisher · View at Google Scholar · View at Scopus
  25. A. G. Rato, J. G. Pedrero, M. A. Martínez, B. Del Rio, P. S. Lazo, and S. Ramos, “Melatonin blocks the activation of estrogen receptor for DNA binding,” The FASEB Journal, vol. 13, no. 8, pp. 857–868, 1999. View at Publisher · View at Google Scholar
  26. A. Bouhoute and G. Leclercq, “Calmodulin decreases the estrogen binding capacity of the estrogen receptor,” Biochemical and Biophysical Research Communications, vol. 227, no. 3, pp. 651–657, 1996. View at Publisher · View at Google Scholar · View at Scopus
  27. B. del Río, J. M. García Pedrero, C. Martínez-Campa, P. Zuazua, P. S. Lazo, and S. Ramos, “Melatonin, an endogenous-specific inhibitor of estrogen receptor alpha via calmodulin,” The Journal of Biological Chemistry, vol. 279, no. 37, pp. 38294–38302, 2004. View at Publisher · View at Google Scholar · View at Scopus
  28. S. T. Wilson, D. E. Blask, and A. M. Lemus-Wilson, “Melatonin augments the sensitivity of MCF-7 human breast cancer cells to tamoxifen in vitro,” The Journal of Clinical Endocrinology and Metabolism, vol. 75, no. 2, pp. 669-670, 1992. View at Publisher · View at Google Scholar · View at Scopus
  29. C. Godson and S. M. Reppert, “The Mel1a melatonin receptor is coupled to parallel signal transduction pathways,” Endocrinology, vol. 138, no. 1, pp. 397–404, 1997. View at Publisher · View at Google Scholar · View at Scopus
  30. S. M. Aronica, W. L. Kraus, and B. S. Katzenellenbogen, “Estrogen action via the cAMP signaling pathway: stimulation of adenylate cyclase and cAMP-regulated gene transcription,” Proceedings of the National Academy of Sciences of the United States of America, vol. 91, no. 18, pp. 8517–8521, 1994. View at Publisher · View at Google Scholar · View at Scopus
  31. S. Cos, C. Martinez-Campa, M. D. Mediavilla, and E. J. Sanchez-Barcelo, “Melatonin modulates aromatase activity in MCF-7 human breast cancer cells,” Journal of Pineal Research, vol. 38, no. 2, pp. 136–142, 2005. View at Publisher · View at Google Scholar · View at Scopus
  32. A. Purohit, L. W. L. Woo, and B. V. L. Potter, “Steroid sulfatase: a pivotal player in estrogen synthesis and metabolism,” Molecular and Cellular Endocrinology, vol. 340, no. 2, pp. 154–160, 2011. View at Publisher · View at Google Scholar · View at Scopus
  33. S. Cos, A. Gonzalez, C. Martinez-Campa, M. Mediavilla, C. Alonso-Gonzalez, and E. Sanchez-Barcelo, “Melatonin as a selective estrogen enzyme modulator,” Current Cancer Drug Targets, vol. 8, no. 8, pp. 691–702, 2008. View at Publisher · View at Google Scholar · View at Scopus
  34. V. Alvarez-García, A. González, C. Martínez-Campa, C. Alonso-González, and S. Cos, “Melatonin modulates aromatase activity and expression in endothelial cells,” Oncology Reports, vol. 29, no. 5, pp. 2058–2064, 2013. View at Publisher · View at Google Scholar · View at Scopus
  35. S. Chottanapund, M. B. M. van Duursen, P. Navasumrit et al., “Anti-aromatase effect of resveratrol and melatonin on hormonal positive breast cancer cells co-cultured with breast adipose fibroblasts,” Toxicology In Vitro, vol. 28, no. 7, pp. 1215–1221, 2014. View at Publisher · View at Google Scholar · View at Scopus
  36. A. González, C. Martínez-Campa, C. Alonso-González, and S. Cos, “Melatonin affects the dynamic steady-state equilibrium of estrogen sulfates in human umbilical vein endothelial cells by regulating the balance between estrogen sulfatase and sulfotransferase,” International Journal of Molecular Medicine, vol. 36, no. 6, pp. 1671–1676, 2015. View at Publisher · View at Google Scholar · View at Scopus
  37. A. González, V. Alvarez-García, C. Martínez-Campa, C. Alonso-González, and S. Cos, “Melatonin promotes differentiation of 3T3-L1 fibroblasts,” Journal of Pineal Research, vol. 52, no. 1, pp. 12–20, 2012. View at Publisher · View at Google Scholar · View at Scopus
  38. V. Alvarez-García, A. González, C. Alonso-González, C. Martínez-Campa, and S. Cos, “Melatonin interferes in the desmoplastic reaction in breast cancer by regulating cytokine production,” Journal of Pineal Research, vol. 52, no. 3, pp. 282–290, 2012. View at Publisher · View at Google Scholar · View at Scopus
  39. V. Alvarez-García, A. González, C. Alonso-González, C. Martínez-Campa, and S. Cos, “Regulation of vascular endothelial growth factor by melatonin in human breast cancer cells,” Journal of Pineal Research, vol. 54, no. 4, pp. 373–380, 2013. View at Publisher · View at Google Scholar · View at Scopus
  40. V. Alvarez-García, A. González, C. Alonso-González, C. Martínez-Campa, and S. Cos, “Antiangiogenic effects of melatonin in endothelial cell cultures,” Microvascular Research, vol. 87, pp. 25–33, 2013. View at Publisher · View at Google Scholar · View at Scopus
  41. S. Cos and D. E. Blask, “Melatonin modulates growth factor activity in MCF-7 human breast cancer cells,” Journal of Pineal Research, vol. 17, no. 1, pp. 25–32, 1994. View at Publisher · View at Google Scholar · View at Scopus
  42. T. M. Molis, L. L. Spriggs, Y. Jupiter, and S. M. Hill, “Melatonin modulation of estrogen-regulated proteins, growth factors, and proto-oncogenes in human breast cancer,” Journal of Pineal Research, vol. 18, no. 2, pp. 93–103, 1995. View at Publisher · View at Google Scholar · View at Scopus
  43. J. K. Colombo, B. V. Jardim-Perasssi, J. P. S. Ferreira et al., “Melatonin differentially modulates NF-κB expression in breast and liver cancer cells,” Anti-Cancer Agents in Medicinal Chemistry, vol. 18, 2018. View at Publisher · View at Google Scholar
  44. J. Hong, N. N. Shah, T. J. Thomas, M. A. Gallo, E. J. Yurkow, and T. Thomas, “Differential effects of estradiol and its analogs on cyclin D1 and CDK4 expression in estrogen receptor positive MCF-7 and estrogen receptor-transfected MCF-10AEwt5 cells,” Oncology Reports, vol. 5, no. 5, pp. 1025–1033, 1998. View at Google Scholar
  45. J. M. Tian, B. Ran, C. L. Zhang, D. M. Yan, and X. H. Li, “Estrogen and progesterone promote breast cancer cell proliferation by inducing cyclin G1 expression,” Brazilian Journal of Medical and Biological Research, vol. 51, no. 3, pp. 1–7, 2018. View at Publisher · View at Google Scholar · View at Scopus
  46. S.-J. In, S.-H. Kim, R.-E. Go, K.-A. Hwang, and K.-C. Choi, “Benzophenone-1 and nonylphenol stimulated MCF-7 breast cancer growth by regulating cell cycle and metastasis-related genes via an estrogen receptor α-dependent pathway,” Journal of Toxicology and Environmental Health, Part A, vol. 78, no. 8, pp. 492–505, 2015. View at Publisher · View at Google Scholar · View at Scopus
  47. M. D. Mediavilla, S. Cos, and E. J. Sánchez-Barceló, “Melatonin increases p 53 and p21WAF1 expression in MCF-7 human breast cancer cells in vitro,” Life Sciences, vol. 65, no. 4, pp. 415–420, 1999. View at Publisher · View at Google Scholar · View at Scopus
  48. S. Proietti, A. Cucina, G. Dobrowolny et al., “Melatonin down-regulates MDM2 gene expression and enhances p 53 acetylation in MCF-7 cells,” Journal of Pineal Research, vol. 57, no. 1, pp. 120–129, 2014. View at Publisher · View at Google Scholar · View at Scopus
  49. L. Ortíz-López, S. Morales-Mulia, G. Ramírez-Rodríguez, and G. Benítez-King, “ROCK-regulated cytoskeletal dynamics participate in the inhibitory effect of melatonin on cancer cell migration,” Journal of Pineal Research, vol. 46, no. 1, pp. 15–21, 2009. View at Publisher · View at Google Scholar · View at Scopus
  50. M. Canel, A. Serrels, M. C. Frame, and V. G. Brunton, “E-cadherin-integrin crosstalk in cancer invasion and metastasis,” Journal of Cell Science, vol. 126, no. 2, pp. 393–401, 2013. View at Publisher · View at Google Scholar · View at Scopus
  51. P. Lissoni, G. Tancini, S. Barni et al., “Treatment of cancer chemotherapy-induced toxicity with the pineal hormone melatonin,” Journal of Pineal Research, vol. 5, no. 2, pp. 126–129, 1997. View at Publisher · View at Google Scholar · View at Scopus
  52. S. Jawed, B. Kim, T. Ottenhof, G. M. Brown, E. S. Werstiuk, and L. P. Niles, “Human melatonin MT1 receptor induction by valproic acid and its effects in combination with melatonin on MCF-7 breast cancer cell proliferation,” European Journal of Pharmacology, vol. 560, no. 1, pp. 17–22, 2007. View at Publisher · View at Google Scholar · View at Scopus
  53. A. Korkmaz, H. Tamura, L. C. Manchester, G. B. Ogden, D. X. Tan, and R. J. Reiter, “Combination of melatonin and a peroxisome proliferator-activated receptor-γ agonist induces apoptosis in a breast cancer cell line,” Journal of Pineal Research, vol. 46, no. 1, pp. 115-116, 2009. View at Publisher · View at Google Scholar · View at Scopus
  54. T. Kisková, C. Ekmekcioglu, M. Garajová et al., “A combination of resveratrol and melatonin exerts chemopreventive effects in N-methyl-N-nitrosourea-induced rat mammary carcinogenesis,” European Journal of Cancer Prevention, vol. 21, no. 2, pp. 163–170, 2012. View at Publisher · View at Google Scholar · View at Scopus
  55. P. Orendáš, P. Kubatka, B. Bojková et al., “Melatonin potentiates the anti-tumour effect of pravastatin in rat mammary gland carcinoma model,” International Journal of Experimental Pathology, vol. 95, no. 6, pp. 401–410, 2014. View at Publisher · View at Google Scholar · View at Scopus
  56. S. Xiang, R. T. Dauchy, A. Hauch et al., “Doxorubicin resistance in breast cancer is driven by light at night-induced disruption of the circadian melatonin signal,” Journal of Pineal Research, vol. 59, no. 1, pp. 60–69, 2015. View at Publisher · View at Google Scholar · View at Scopus
  57. C. Ma, L. X. Li, Y. Zhang et al., “Protective and sensitive effects of melatonin combined with Adriamycin on ER+ (estrogen receptor) breast cancer,” European Journal of Gynaecological Oncology, vol. 36, no. 2, pp. 197–202, 2015. View at Google Scholar
  58. P. A. Kosar, M. Naziroglu, I. S. Ovey, and B. Cig, “Synergic effects of doxorubicin and melatonin on apoptosis and mitochondrial oxidative stress in MCF-7 breast cancer cells: involvement of TRPV1 channels,” The Journal of Membrane Biology, vol. 249, no. 1-2, pp. 129–140, 2016. View at Publisher · View at Google Scholar · View at Scopus
  59. C. Alonso-González, J. Menéndez-Menéndez, A. González-González, A. González, S. Cos, and C. Martínez-Campa, “Melatonin enhances the apoptotic effects and modulates the changes in gene expression induced by docetaxel in MCF-7 human breast cancer cells,” International Journal of Oncology, vol. 52, no. 2, pp. 560–570, 2018. View at Publisher · View at Google Scholar · View at Scopus
  60. K. L. Koenig, R. E. Goans, R. J. Hatchett et al., “Medical treatment of radiological casualties: current concepts,” Annals of Emergency Medicine, vol. 45, no. 6, pp. 643–652, 2005. View at Publisher · View at Google Scholar · View at Scopus
  61. Vijayalaxmi, R. J. Reiter, D. X. Tan, T. S. Herman, and C. R. Thomas Jr, “Melatonin as a radioprotective agent: a review,” International Journal of Radiation Oncology Biology Physics, vol. 59, no. 3, pp. 639–653, 2004. View at Publisher · View at Google Scholar · View at Scopus
  62. S. J. Veuger, N. J. Curtin, C. J. Richardson, G. C. Smith, and B. W. Durkacz, “Radiosensitization and DNA repair inhibition by the combined use of novel inhibitors of DNA-dependent protein kinase and poly(ADP-ribose) polymerase-1,” Cancer Research, vol. 63, no. 18, pp. 6008–6015, 2003. View at Google Scholar
  63. A. J. Davis, B. P. C. Chen, and D. J. Chen, “DNA-PK: a dynamic enzyme in a versatile DSB repair pathway,” DNA Repair, vol. 17, pp. 21–29, 2014. View at Publisher · View at Google Scholar · View at Scopus
  64. S. S. Jang, W. D. Kim, and W. Y. Park, “Melatonin exerts differential actions on X-ray radiation-induced apoptosis in normal mice splenocytes and Jurkat leukemia cells,” Journal of Pineal Research, vol. 47, no. 2, pp. 147–155, 2009. View at Publisher · View at Google Scholar · View at Scopus
  65. C. Alonso-González, A. González, C. Martínez-Campa, J. Gómez-Arozamena, and S. Cos, “Melatonin sensitizes human breast cancer cells to ionizing radiation by downregulating proteins involved in double-strand DNA break repair,” Journal of Pineal Research, vol. 58, no. 2, pp. 189–197, 2015. View at Publisher · View at Google Scholar · View at Scopus
  66. C. Alonso-González, A. González, C. Martínez-Campa et al., “Melatonin enhancement of the radiosensitivity of human breast cancer cells is associated with the modulation of proteins involved in estrogen biosynthesis,” Cancer Letters, vol. 370, no. 1, pp. 145–152, 2016. View at Publisher · View at Google Scholar · View at Scopus
  67. M. Ishitobi, M. Shiba, T. Nakayama et al., “Treatment sequence of aromatase inhibitors and radiotherapy and long-term outcomes of breast cancer patients,” Anticancer Research, vol. 34, no. 8, pp. 4311–4314, 2014. View at Google Scholar
  68. Z. Cai, W. Chen, J. Zhang, and H. Li, “Androgen receptor: what we know and what we expect in castration-resistant prostate cancer,” International Urology and Nephrology, 2018. View at Publisher · View at Google Scholar
  69. L. Debeljuk, V. M. Feder, and O. A. Paulucci, “Effects of melatonin on changes induced by castration and testosterone in sexual structures of male rats,” Endocrinology, vol. 87, no. 6, pp. 1358–1360, 1970. View at Publisher · View at Google Scholar · View at Scopus
  70. F. Peat and G. A. Kinson, “Testicular steroidogenesis in vitro in the rat in response to blinding, pinealectomy and to the addition of melatonin,” Steroids, vol. 17, no. 1-5, pp. 251–264, 1971. View at Publisher · View at Google Scholar · View at Scopus
  71. C. Bartsch, H. Bartsch, S. H. Flüchter, A. Attanasio, and D. Gupta, “Evidence for modulation of melatonin secretion in men with benign and malignant tumors of the prostate: relationship with the pituitary hormones,” Journal of Pineal Research, vol. 2, no. 2, pp. 121–132, 1985. View at Publisher · View at Google Scholar · View at Scopus
  72. J. G. Toma, H. M. Amerongen, S. C. Hennes, M. G. O'Brien, W. A. McBlain, and G. R. Buzzell, “Effects of olfactory bulbectomy, melatonin, and/or pinealectomy on three sublines of the Dunning R3327 rat prostatic adenocarcinoma,” Journal of Pineal Research, vol. 4, no. 3, pp. 321–338, 1987. View at Publisher · View at Google Scholar · View at Scopus
  73. C. Bartsch, H. Bartsch, A. Schmidt, S. Ilg, K. H. Bichler, and S. H. Flüchter, “Melatonin and 6-sulfatoxymelatonin circadian rhythms in serum and urine of primary prostate cancer patients: evidence for reduced pineal activity and relevance of urinary determinations,” Clinica Chimica Acta, vol. 209, no. 3, pp. 153–167, 1992. View at Publisher · View at Google Scholar · View at Scopus
  74. P. Lissoni, M. Cazzaniga, G. Tancini et al., “Reversal of clinical resistance to LHRH analogue in metastatic prostate cancer by the pineal hormone melatonin: efficacy of LHRH analogue plus melatonin in patients progressing on LHRH analogue alone,” European Urology, vol. 31, no. 2, pp. 178–181, 1997. View at Publisher · View at Google Scholar · View at Scopus
  75. Z. Lupowitz and N. Zisapel, “Hormonal interactions in human prostate tumor LNCaP cells,” The Journal of Steroid Biochemistry and Molecular Biology, vol. 68, no. 1-2, pp. 83–88, 1999. View at Publisher · View at Google Scholar · View at Scopus
  76. R. M. Moretti, M. M. Marelli, R. Maggi, D. Dondi, M. Motta, and P. Limonta, “Antiproliferative action of melatonin on human prostate cancer LNCaP cells,” Oncology Reports, vol. 7, no. 2, pp. 347–351, 2000. View at Google Scholar
  77. M. M. Marelli, P. Limonta, R. Maggi, M. Motta, and R. M. Moretti, “Growth-inhibitory activity of melatonin on human androgen-independent DU 145 prostate cancer cells,” The Prostate, vol. 45, no. 3, pp. 238–244, 2000. View at Publisher · View at Google Scholar
  78. A. Rimler, Z. Culig, G. Levy-Rimler et al., “Melatonin elicits nuclear exclusion of the human androgen receptor and attenuates its activity,” Prostate, vol. 49, no. 2, pp. 145–154, 2001. View at Publisher · View at Google Scholar · View at Scopus
  79. Z. Lupowitz, A. Rimler, and N. Zisapel, “Evaluation of signal transduction pathways mediating the nuclear exclusion of the androgen receptor by melatonin,” Cellular and Molecular Life Sciences, vol. 58, no. 14, pp. 2129–2135, 2001. View at Publisher · View at Google Scholar · View at Scopus
  80. S. W. F. Siu, K. W. Lau, P. C. Tam, and S. Y. W. Shiu, “Melatonin and prostate cancer cell proliferation: interplay with castration, epidermal growth factor, and androgen sensitivity,” The Prostate, vol. 52, no. 2, pp. 106–122, 2002. View at Publisher · View at Google Scholar · View at Scopus
  81. R. M. Sainz, J. C. Mayo, D. X. Tan, J. León, L. Manchester, and R. J. Reiter, “Melatonin reduces prostate cancer cell growth leading to neuroendocrine differentiation via a receptor and PKA independent mechanism,” The Prostate, vol. 63, no. 1, pp. 29–43, 2005. View at Publisher · View at Google Scholar · View at Scopus
  82. R. M. Sainz, R. J. Reiter, D. X. Tan et al., “Critical role of glutathione in melatonin enhancement of tumor necrosis factor and ionizing radiation-induced apoptosis in prostate cancer cells in vitro,” Journal of Pineal Research, vol. 45, no. 3, pp. 258–270, 2008. View at Publisher · View at Google Scholar · View at Scopus
  83. S. Y. W. Shiu, W. Y. Leung, C. W. Tam, V. W. S. Liu, and K.-M. Yao, “Melatonin MT1 receptor-induced transcriptional up-regulation of p27Kip1 in prostate cancer antiproliferation is mediated via inhibition of constitutively active nuclear factor kappa B (NF-κb): potential implications on prostate cancer chemoprevention and therapy,” Journal of Pineal Research, vol. 54, no. 1, pp. 69–79, 2013. View at Publisher · View at Google Scholar · View at Scopus
  84. S. S. Joo and Y. M. Yoo, “Melatonin induces apoptotic death in LNCaP cells via p38 and JNK pathways: therapeutic implications for prostate cancer,” Journal of Pineal Research, vol. 47, no. 1, pp. 8–14, 2009. View at Publisher · View at Google Scholar · View at Scopus
  85. J.-W. Park, M.-S. Hwang, S.-I. Suh, and W.-K. Baek, “Melatonin down-regulates HIF-1α expression through inhibition of protein translation in prostate cancer cells,” Journal of Pineal Research, vol. 46, no. 4, pp. 415–421, 2009. View at Publisher · View at Google Scholar · View at Scopus
  86. B. Jung-Hynes, T. L. Schmit, S. R. Reagan-Shaw, I. A. Siddiqui, H. Mukhtar, and N. Ahmad, “Melatonin, a novel Sirt1 inhibitor, imparts antiproliferative effects against prostate cancer in vitro in culture and in vivo in TRAMP model,” Journal of Pineal Research, vol. 50, no. 2, pp. 140–149, 2011. View at Publisher · View at Google Scholar · View at Scopus
  87. D. Hevia, P. Gonzalez-Menendez, M. Fernandez-Fernandez et al., “Melatonin decreases glucose metabolism in prostate cancer cells: a 13C stable isotope-resolved metabolomic study,” International Journal of Molecular Sciences, vol. 18, no. 8, 2017. View at Publisher · View at Google Scholar · View at Scopus
  88. J. C. Mayo, D. Hevia, I. Quiros-Gonzalez et al., “IGFBP3 and MAPK/ERK signaling mediates melatonin-induced antitumor activity in prostate cancer,” Journal of Pineal Research, vol. 62, no. 1, article e12373, 2017. View at Publisher · View at Google Scholar · View at Scopus
  89. R. Paroni, L. Terraneo, F. Bonomini et al., “Antitumour activity of melatonin in a mouse model of human prostate cancer: relationship with hypoxia signalling,” Journal of Pineal Research, vol. 57, no. 1, pp. 43–52, 2014. View at Publisher · View at Google Scholar · View at Scopus
  90. E. J. Sohn, G. Won, J. Lee, S. Lee, and S. H. Kim, “Upregulation of miRNA3195 and miRNA374b mediates the anti-angiogenic properties of melatonin in hypoxic PC-3 prostate cancer cells,” Journal of Cancer, vol. 6, no. 1, pp. 19–28, 2015. View at Publisher · View at Google Scholar · View at Scopus
  91. B. Jung-Hynes, W. Huang, R. J. Reiter, and N. Ahmad, “Melatonin resynchronizes dysregulated circadian rhythm circuitry in human prostate cancer cells,” Journal of Pineal Research, vol. 49, no. 1, pp. 60–68, 2010. View at Publisher · View at Google Scholar · View at Scopus
  92. A. Rodriguez-Garcia, J. C. Mayo, D. Hevia, I. Quiros-Gonzalez, M. Navarro, and R. M. Sainz, “Phenotypic changes caused by melatonin increased sensitivity of prostate cancer cells to cytokine-induced apoptosis,” Journal of Pineal Research, vol. 54, no. 1, pp. 33–45, 2013. View at Publisher · View at Google Scholar · View at Scopus
  93. I. Kloog, A. Haim, R. G. Stevens, and B. A. Portnov, “Global co-distribution of light at night (LAN) and cancers of prostate, colon, and lung in men,” Chronobiology International, vol. 26, no. 1, pp. 108–125, 2009. View at Publisher · View at Google Scholar · View at Scopus
  94. M. E. Parent, M. el-Zein, M. C. Rousseau, J. Pintos, and J. Siemiatycki, “Night work and the risk of cancer among men,” American Journal of Epidemiology, vol. 176, no. 9, pp. 751–759, 2012. View at Publisher · View at Google Scholar · View at Scopus
  95. L. G. Sigurdardottir, S. C. Markt, J. R. Rider et al., “Urinary melatonin levels, sleep disruption, and risk of prostate cancer in elderly men,” European Urology, vol. 67, no. 2, pp. 191–194, 2015. View at Publisher · View at Google Scholar · View at Scopus
  96. F. Gu, H. Zhang, P. L. Hyland et al., “Inherited variation in circadian rhythm genes and risks of prostate cancer and three other cancer sites in combined cancer consortia,” International Journal of Cancer, vol. 141, no. 9, pp. 1794–1802, 2017. View at Publisher · View at Google Scholar · View at Scopus
  97. K. K. Tsilidis, N. E. Allen, T. J. Key et al., “Oral contraceptive use and reproductive factors and risk of ovarian cancer in the European Prospective Investigation into Cancer and Nutrition,” British Journal of Cancer, vol. 105, no. 9, pp. 1436–1442, 2011. View at Publisher · View at Google Scholar · View at Scopus
  98. H. Schock, H. M. Surcel, A. Zeleniuch-Jacquotte et al., “Early pregnancy sex steroids and maternal risk of epithelial ovarian cancer,” Endocrine-Related Cancer, vol. 21, no. 6, pp. 831–844, 2014. View at Publisher · View at Google Scholar · View at Scopus
  99. Y. Kikuchi, T. Kita, M. Miyauchi, I. Iwano, and K. Kato, “Inhibition of human ovarian cancer cell proliferation in vitro by neuroendocrine hormones,” Gynecologic Oncology, vol. 32, no. 1, pp. 60–64, 1989. View at Publisher · View at Google Scholar · View at Scopus
  100. H. Tamura, Y. Nakamura, A. Korkmaz et al., “Melatonin and the ovary: physiological and pathophysiological implications,” Fertility and Sterility, vol. 92, no. 1, pp. 328–343, 2009. View at Publisher · View at Google Scholar · View at Scopus
  101. R. Sandyk, P. G. Anastasiadis, P. A. Anninos, and N. Tsagas, “Is the pineal gland involved in the pathogenesis of endometrial carcinoma,” International Journal of Neuroscience, vol. 62, no. 1-2, pp. 89–96, 1991. View at Publisher · View at Google Scholar · View at Scopus
  102. E. M. Poole, E. S. Schernhammer, and S. S. Tworoger, “Rotating night shift work and risk of ovarian cancer,” Cancer Epidemiology, Biomarkers and Prevention, vol. 20, no. 5, pp. 934–938, 2011. View at Publisher · View at Google Scholar · View at Scopus
  103. E. M. Poole, E. Schernhammer, L. Mills, S. E. Hankinson, and S. S. Tworoger, “Urinary melatonin and risk of ovarian cancer,” Cancer Causes and Control, vol. 26, no. 10, pp. 1501–1506, 2015. View at Publisher · View at Google Scholar · View at Scopus
  104. M. Zhao, J. Wan, K. Zeng et al., “The reduction in circulating melatonin level may contribute to the pathogenesis of ovarian cancer: a retrospective study,” Journal of Cancer, vol. 7, no. 7, pp. 831–836, 2016. View at Publisher · View at Google Scholar · View at Scopus
  105. P. Lissoni, A. Ardizzoia, S. Barni, G. Tancini, and M. Muttini, “Immunotherapy with subcutaneous low dose interleukin-2 plus melatonin as salvage therapy of heavily chemotherapy-pretreated ovarian cancer,” Oncology Reports, vol. 3, no. 5, pp. 947–949, 1996. View at Google Scholar
  106. J. Petranka, W. Baldwin, J. Biermann, S. Jayadev, J. C. Barrett, and E. Murphy, “The oncostatic action of melatonin in an ovarian carcinoma cell line,” Journal of Pineal Research, vol. 26, no. 3, pp. 129–136, 1999. View at Publisher · View at Google Scholar · View at Scopus
  107. O. Treeck, C. Haldar, and O. Ortmann, “Antiestrogens modulate MT1 melatonin receptor expression in breast and ovarian cancer cell lines,” Oncology Reports, vol. 15, no. 1, pp. 231–235, 2006. View at Google Scholar
  108. K. Jablonska, B. Pula, A. Zemla et al., “Expression of the MT1 melatonin receptor in ovarian cancer cells,” International Journal of Molecular Sciences, vol. 15, no. 12, pp. 23074–23089, 2014. View at Publisher · View at Google Scholar · View at Scopus
  109. L. G. A. Chuffa, B. A. Fioruci-Fontanelli, L. O. Mendes et al., “Characterization of chemically induced ovarian carcinomas in an ethanol-preferring rat model: influence of long-term melatonin treatment,” PLoS One, vol. 8, no. 12, article e81676, 2013. View at Publisher · View at Google Scholar · View at Scopus
  110. G. M. Ferreira, M. Martinez, I. C. C. Camargo, R. F. Domeniconi, F. E. Martinez, and L. G. A. Chuffa, “Melatonin attenuates Her-2, p38 MAPK, p-AKT, and mTOR levels in ovarian carcinoma of ethanol-preferring rats,” Journal of Cancer, vol. 5, no. 9, pp. 728–735, 2014. View at Publisher · View at Google Scholar · View at Scopus
  111. L. G. A. Chuffa, B. A. Fioruci-Fontanelli, L. O. Mendes et al., “Melatonin attenuates the TLR4-mediated inflammatory response through MyD88- and TRIF-dependent signaling pathways in an in vivo model of ovarian cancer,” BMC Cancer, vol. 15, no. 1, p. 34, 2015. View at Publisher · View at Google Scholar · View at Scopus
  112. L. G. Chuffa, M. S. Alves, M. Martinez et al., “Apoptosis is triggered by melatonin in an in vivo model of ovarian carcinoma,” Endocrine-Related Cancer, vol. 23, no. 2, pp. 65–76, 2016. View at Publisher · View at Google Scholar · View at Scopus
  113. L. G. A. Chuffa, L. A. Lupi Júnior, F. R. F. Seiva et al., “Quantitative proteomic profiling reveals that diverse metabolic pathways are influenced by melatonin in an in vivo model of ovarian carcinoma,” Journal of Proteome Research, vol. 15, no. 10, pp. 3872–3882, 2016. View at Publisher · View at Google Scholar · View at Scopus
  114. Y. R. Zonta, M. Martinez, I. C. Camargo et al., “Melatonin reduces angiogenesis is serous papillary ovarian carcinoma of ethanol-preferring rats,” International Journal of Molecular Sciences, vol. 18, no. 4, 2017. View at Publisher · View at Google Scholar · View at Scopus
  115. C. J. Shen, C. C. Chang, Y. T. Chen, C. S. Lai, and Y. C. Hsu, “Melatonin suppresses the growth of ovarian cancer cell lines (OVCAR-429 and PA-1) and potentiates the effect of G1 arrest by targeting CDKs,” International Journal of Molecular Sciences, vol. 17, no. 2, 2016. View at Publisher · View at Google Scholar · View at Scopus
  116. M. Akbarzadeh, A. A. Movassaghpour, H. Ghanbari et al., “The potential therapeutic effect of melatonin on human ovarian cancer by inhibition of invasion and migration of cancer stem cells,” Scientific Reports, vol. 7, no. 1, article 17062, 2017. View at Publisher · View at Google Scholar · View at Scopus
  117. H. Bartsch, A. Buchberger, H. Franz et al., “Effect of melatonin and pineal extracts on human ovarian and mammary tumor cells in a chemosensitivity assay,” Life Sciences, vol. 67, no. 24, pp. 2953–2960, 2000. View at Publisher · View at Google Scholar · View at Scopus
  118. M. Futagami, S. Sato, T. Sakamoto, Y. Yokoyama, and Y. Saito, “Effects of melatonin on the proliferation and cis-diamminedichloroplatinum (CDDP) sensitivity of cultured human ovarian cancer cells,” Gynecologic Oncology, vol. 82, no. 3, pp. 544–549, 2001. View at Publisher · View at Google Scholar · View at Scopus
  119. J.-H. Kim, S.-J. Jeong, B. Kim, S.-M. Yun, D. Y. Choi, and S.-H. Kim, “Melatonin synergistically enhances cisplatin-induced apoptosis via the dephosphorylation of ERK/p90 ribosomal S6 kinase/heat shock protein 27 in SK-OV-3 cells,” Journal of Pineal Research, vol. 52, no. 2, pp. 244–252, 2012. View at Publisher · View at Google Scholar · View at Scopus
  120. H. Jang, O. H. Lee, Y. Lee et al., “Melatonin prevents cisplatin-induced primordial follicle loss via suppression of PTEN/AKT/FOXO3a pathway activation in the mouse ovary,” Journal of Pineal Research, vol. 60, no. 3, pp. 336–347, 2016. View at Publisher · View at Google Scholar · View at Scopus
  121. H. Jang, Y. Na, K. Hong et al., “Synergistic effect of melatonin and ghrelin in preventing cisplatin-induced ovarian damage via regulation of FOXO3a phosphorylation and binding to the p27kip1 promoter in primordial follicles,” Journal of Pineal Research, vol. 63, no. 3, 2017. View at Publisher · View at Google Scholar · View at Scopus
  122. R. S. Barberino, V. G. Menezes, A. E. A. S. Ribeiro et al., “Melatonin protects against cisplatin-induced ovarian damage in mice via the MT1 receptor and antioxidant activity,” Biology of Reproduction, vol. 96, no. 6, pp. 1244–1255, 2017. View at Publisher · View at Google Scholar · View at Scopus
  123. A. Zemła, I. Grzegorek, P. Dzięgiel, and K. Jabłońska, “Melatonin synergizes the chemotherapeutic effect of cisplatin in ovarian cancer cells independently of MT1 melatonin receptors,” In Vivo, vol. 31, no. 5, pp. 801–809, 2018. View at Publisher · View at Google Scholar · View at Scopus
  124. M. Akbarzadeh, M. Nouri, M. V. Banekohal et al., “Effects of combination of melatonin and laser irradiation on ovarian cancer cells and endothelial lineage viability,” Lasers in Medical Science, vol. 31, no. 8, pp. 1565–1572, 2016. View at Publisher · View at Google Scholar · View at Scopus
  125. K. Jablonska, B. Pula, A. Zemla et al., “Expression of melatonin receptor MT1 in cells of human invasive ductal breast carcinoma,” Journal of Pineal Research, vol. 54, no. 3, pp. 334–345, 2013. View at Publisher · View at Google Scholar · View at Scopus
  126. P. T. Ram, J. Dai, L. Yuan et al., “Involvement of the mt1 melatonin receptor in human breast cancer,” Cancer Letters, vol. 179, no. 2, pp. 141–150, 2002. View at Publisher · View at Google Scholar · View at Scopus
  127. J. M. Soares Jr., M. I. Masana, C. Erşahin, and M. L. Dubocovich, “Functional melatonin receptors in rat ovaries at various stages of the estrous cycle,” Journal of Pharmacology and Experimental Therapeutics, vol. 306, no. 2, pp. 694–702, 2003. View at Publisher · View at Google Scholar · View at Scopus
  128. M. Baratta and C. Tamanini, “Effect of melatonin on the in vitro secretion of progesterone and estradiol 17β by ovine granulosa cells,” Acta Endocrinologica, vol. 127, no. 4, pp. 366–370, 1992. View at Publisher · View at Google Scholar
  129. A. V. Sirotkin, “Direct influence of melatonin on steroid, nonapeptide hormones, and cyclic nucleotide secretion by granulosa cells isolated from porcine ovaries,” Journal of Pineal Research, vol. 17, no. 3, pp. 112–117, 1994. View at Publisher · View at Google Scholar · View at Scopus
  130. J. Bódis, M. Koppán, L. Kornya, H. R. Tinneberg, and A. Török, “Influence of melatonin on basal and gonadotropin-stimulated progesterone and estradiol secretion of cultured human granulosa cells and in the superfused granulosa cell system,” Gynecologic and Obstetric Investigation, vol. 52, no. 3, pp. 198–202, 2001. View at Publisher · View at Google Scholar · View at Scopus
  131. H. Tamura, Y. Nakamura, S. Takiguchi et al., “Melatonin directly suppresses steroid production by preovulatory follicles in the cyclic hamster,” Journal of Pineal Research, vol. 25, no. 3, pp. 135–141, 1998. View at Publisher · View at Google Scholar · View at Scopus
  132. E. S. Schernhammer, B. Rosner, W. C. Willett, F. Laden, G. A. Colditz, and S. E. Hankinson, “Epidemiology of urinary melatonin in women and its relation to other hormones and night work,” Cancer Epidemiology Biomarkers & Prevention, vol. 13, no. 6, pp. 936–943, 2004. View at Google Scholar
  133. X. Ren, X. Wu, S. G. Hillier et al., “Local estrogen metabolism in epithelial ovarian cancer suggests novel targets for therapy,” The Journal of Steroid Biochemistry and Molecular Biology, vol. 150, pp. 54–63, 2015. View at Publisher · View at Google Scholar · View at Scopus
  134. F. Mungenast, S. Aust, I. Vergote et al., “Clinical significance of the estrogen-modifying enzymes steroid sulfatase and estrogen sulfotransferase in epithelial ovarian cancer,” Oncology Letters, vol. 13, no. 6, pp. 4047–4054, 2017. View at Publisher · View at Google Scholar · View at Scopus
  135. E. Damian and O. Ianäs, “Inhibition of testosterone-induced prostate growth in the rat by melatonin-free pineal extract,” Endocrinologie, vol. 17, no. 4, pp. 241–244, 1979. View at Google Scholar
  136. S. Persengiev and J. Kehajova, “Inhibitory action of melatonin and structurally related compounds on testosterone production by mouse Leydig cells in vitro,” Cell Biochemistry and Function, vol. 9, no. 4, pp. 281–286, 1991. View at Publisher · View at Google Scholar · View at Scopus
  137. M. B. Frungieri, A. Mayerhofer, K. Zitta, O. P. Pignataro, R. S. Calandra, and S. I. Gonzalez-Calvar, “Direct effect of melatonin on Syrian hamster testes: melatonin subtype 1a receptors, inhibition of androgen production, and interaction with the local corticotropin-releasing hormone system,” Endocrinology, vol. 146, no. 3, pp. 1541–1552, 2005. View at Publisher · View at Google Scholar · View at Scopus
  138. A. Mukherjee and C. Haldar, “Photoperiodic regulation of melatonin membrane receptor (MT1R) expression and steroidogenesis in testis of adult golden hamster, Mesocricetus auratus,” Journal of Photochemistry and Photobiology B: Biology, vol. 140, pp. 374–380, 2014. View at Publisher · View at Google Scholar · View at Scopus
  139. F. Qin, J. Zhang, L. Zan et al., “Inhibitory effect of melatonin on testosterone synthesis is mediated via GATA-4/SF-1 transcription factors,” Reproductive Biomedicine Online, vol. 31, no. 5, pp. 638–646, 2015. View at Publisher · View at Google Scholar · View at Scopus
  140. K. Papantoniou, O. J. Pozo, A. Espinosa et al., “Increased and mistimed sex hormone production in night shift workers,” Cancer Epidemiology Biomarkers & Prevention, vol. 24, no. 5, pp. 854–863, 2015. View at Publisher · View at Google Scholar · View at Scopus
  141. P. P. Banerjee, S. Banerjee, T. R. Brown, and B. R. Zirkin, “Androgen action in prostate function and disease,” American Journal of Clinical and Experimental Urology, vol. 6, no. 2, pp. 62–77, 2018. View at Google Scholar
  142. D. Hettel, A. Zhang, M. Alyamani, M. Berk, and N. Sharifi, “AR signaling in prostate cancer regulates a feed-forward mechanism of androgen synthesis by way of HSD3B1 upregulation,” Endocrinology, vol. 159, no. 8, pp. 2884–2890, 2018. View at Publisher · View at Google Scholar
  143. L. G. A. Chuffa, F. R. F. Seiva, W. J. Fávaro et al., “Melatonin and ethanol intake exert opposite effects on circulating estradiol and progesterone and differentially regulate sex steroid receptors in the ovaries, oviducts, and uteri of adult rats,” Reproductive Toxicology, vol. 39, pp. 40–49, 2013. View at Publisher · View at Google Scholar · View at Scopus
  144. T. Abbas and A. Dutta, “p21 in cancer: intricate networks and multiple activities,” Nature Reviews Cancer, vol. 9, no. 6, pp. 400–414, 2009. View at Publisher · View at Google Scholar · View at Scopus
  145. S. Cos, J. Recio, and E. J. Sánchez-Barceló, “Modulation of the length of the cell cycle time of MCF-7 human breast cancer cells by melatonin,” Life Sciences, vol. 58, no. 9, pp. 811–816, 1996. View at Publisher · View at Google Scholar · View at Scopus
  146. L. Mao, L. Yuan, L. M. Slakey, F. E. Jones, M. E. Burow, and S. M. Hill, “Inhibition of breast cancer cell invasion by melatonin is mediated through regulation of the p38 mitogen-activated protein kinase signaling pathway,” Breast Cancer Research, vol. 12, no. 6, article R107, 2010. View at Publisher · View at Google Scholar · View at Scopus
  147. A. Rimler, H. Matzkin, and N. Zisapel, “Cross talk between melatonin and TGFβ1 in human benign prostate epithelial cells,” Prostate, vol. 40, no. 4, pp. 211–217, 1999. View at Publisher · View at Google Scholar
  148. A. Cucina, S. Proietti, F. D’Anselmi et al., “Evidence for a biphasic apoptotic pathway induced by melatonin in MCF-7 breast cancer cells,” Journal of Pineal Research, vol. 46, no. 2, pp. 172–180, 2009. View at Publisher · View at Google Scholar · View at Scopus
  149. M. A. A. el-Aziz, H. A. Hassan, M. H. Mohamed, A. R. M. A. Meki, S. K. H. Abdel-Ghaffar, and M. R. Hussein, “The biochemical and morphological alterations following administration of melatonin, retinoic acid and Nigella sativa in mammary carcinoma: an animal model,” International Journal of Experimental Pathology, vol. 86, no. 6, pp. 383–396, 2005. View at Publisher · View at Google Scholar · View at Scopus
  150. J. Wang, X. Xiao, Y. Zhang et al., “Simultaneous modulation of COX-2, p300, Akt, and Apaf-1 signaling by melatonin to inhibit proliferation and induce apoptosis in breast cancer cells,” Journal of Pineal Research, vol. 53, no. 1, pp. 77–90, 2012. View at Publisher · View at Google Scholar · View at Scopus
  151. C. H. Kim and Y. M. Yoo, “Melatonin induces apoptotic cell death via p53 in LNCaP cells,” Korean Journal of Physiology and Pharmacology, vol. 14, no. 6, pp. 365–369, 2010. View at Publisher · View at Google Scholar · View at Scopus
  152. P. Lissoni, F. Rovelli, F. Malugani, R. Bucovec, A. Conti, and G. J. Maestroni, “Anti-angiogenic activity of melatonin in advanced cancer patients,” Neuro Endocrinology Letters, vol. 22, no. 1, pp. 45–47, 2001. View at Google Scholar
  153. P. Cui, Z. Luo, H. Zhang et al., “Effect and mechanism of melatonin’s action on the proliferation of human umbilical vein endothelial cells,” Journal of Pineal Research, vol. 41, no. 4, pp. 358–362, 2006. View at Publisher · View at Google Scholar · View at Scopus
  154. A. González-González, A. González, C. Alonso-González, J. Menéndez-Menéndez, C. Martínez-Campa, and S. Cos, “Complementary actions of melatonin on angiogenic factors, the angiopoietin/Tie2 axis and VEGF, in co-cultures of human endothelial and breast cancer cells,” Oncology Reports, vol. 39, no. 1, pp. 433–441, 2018. View at Publisher · View at Google Scholar · View at Scopus
  155. B. V. Jardim-Perassi, A. S. Arbab, L. C. Ferreira et al., “Effect of melatonin on tumor growth and angiogenesis in xenograft model of breast cancer,” PLoS One, vol. 9, no. 1, article e85311, 2014. View at Publisher · View at Google Scholar · View at Scopus
  156. J. H. M. Marques, A. L. Mota, J. G. Oliveira et al., “Melatonin restrains angiogenic factors in triple negative breast cancer by targeting miR-152-3p: in vivo and in vitro studies,” Life Sciences, vol. 208, pp. 131–138, 2018. View at Publisher · View at Google Scholar
  157. P. Lissoni, S. Barni, S. Meregalli et al., “Modulation of cancer endocrine therapy by melatonin: a phase II study of tamoxifen plus melatonin in metastatic breast cancer patients progressing under tamoxifen alone,” British Journal of Cancer, vol. 71, no. 4, pp. 854–856, 1995. View at Publisher · View at Google Scholar · View at Scopus
  158. S. Cos, R. Fernández, A. Güezmes, and E. J. Sánchez-Barceló, “Influence of melatonin on invasive and metastatic properties of MCF-7 human breast cancer cells,” Cancer Research, vol. 58, no. 19, pp. 4383–4390, 1998. View at Google Scholar
  159. T. F. Borin, A. S. Arbab, G. B. Gelaleti et al., “Melatonin decreases breast cancer metastasis by modulating Rho-associated kinase protein-1 expression,” Journal of Pineal Research, vol. 60, no. 1, pp. 3–15, 2016. View at Publisher · View at Google Scholar · View at Scopus
  160. L. Mao, R. T. Dauchy, D. E. Blask et al., “Circadian gating of epithelial-to-mesenchymal transition in breast cancer cells via melatonin-regulation of GSK3β,” Molecular Endocrinology, vol. 26, no. 11, pp. 1808–1820, 2012. View at Publisher · View at Google Scholar · View at Scopus
  161. N. do Nascimento Gonçalves, J. Colombo, J. R. Lopes et al., “Effect of melatonin in epithelial mesenchymal transition markers and invasive properties of breast cancer stem cells of canine and human cell lines,” PLoS One, vol. 11, no. 3, article e0150407, 2016. View at Publisher · View at Google Scholar · View at Scopus
  162. L. Mao, W. Summers, S. Xiang et al., “Melatonin represses metastasis in Her2-postive human breast cancer cells by suppressing RSK2 expression,” Molecular Cancer Research, vol. 14, no. 11, pp. 1159–1169, 2016. View at Publisher · View at Google Scholar · View at Scopus
  163. P. Lissoni, S. Barni, M. Mandalà et al., “Decreased toxicity and increased efficacy of cancer chemotherapy using the pineal hormone melatonin in metastatic solid tumour patients with poor clinical status,” European Journal of Cancer, vol. 35, no. 12, pp. 1688–1692, 1999. View at Publisher · View at Google Scholar · View at Scopus
  164. P. Lissoni, G. Tancini, F. Paolorossi et al., “Chemoneuroendocrine therapy of metastatic breast cancer with persistent thrombocytopenia with weekly low-dose epirubicin plus melatonin: a phase II study,” Journal of Pineal Research, vol. 26, no. 3, pp. 169–173, 1999. View at Publisher · View at Google Scholar · View at Scopus
  165. K. Greish, I. Sanada, Saad Ael-D et al., “Protective effect of melatonin on human peripheral blood hematopoeitic stem cells against doxorubicin cytotoxicity,” Anticancer Research, vol. 25, no. 6B, pp. 4245–4248, 2005. View at Google Scholar
  166. Z. Nahleh, J. Pruemer, J. Lafollette, and S. Sweany, “Melatonin, a promising role in taxane-related neuropathy,” Clinical Medicine Insights: Oncology, vol. 4, pp. 35–41, 2010. View at Publisher · View at Google Scholar
  167. H. F. Galley, B. McCormick, K. L. Wilson, D. A. Lowes, L. Colvin, and C. Torsney, “Melatonin limits paclitaxel-induced mitochondrial dysfunction in vitro and protects against paclitaxel-induced neuropathic pain in the rat,” Journal of Pineal Research, vol. 63, no. 4, article e12444, 2017. View at Publisher · View at Google Scholar · View at Scopus
  168. K. M. Eck, L. Yuan, L. Duffy et al., “A sequential treatment regimen with melatonin and all-trans retinoic acid induces apoptosis in MCF-7 tumour cells,” British Journal of Cancer, vol. 77, no. 12, pp. 2129–2137, 1998. View at Publisher · View at Google Scholar · View at Scopus
  169. M. Margheri, N. Pacini, A. Tani et al., “Combined effects of melatonin and all-trans retinoic acid and somatostatin on breast cancer cell proliferation and death: molecular basis for the anticancer effect of these molecules,” European Journal of Pharmacology, vol. 681, no. 1–3, pp. 34–43, 2012. View at Publisher · View at Google Scholar · View at Scopus
  170. E. Nooshinfar, D. Bashash, A. Safaroghli-Azar et al., “Melatonin promotes ATO-induced apoptosis in MCF-7 cells: proposing novel therapeutic potential for breast cancer,” Biomedicine & Pharmacotherapy, vol. 83, pp. 456–465, 2016. View at Publisher · View at Google Scholar · View at Scopus
  171. A. Kothari, A. Borges, A. Ingle, and L. Kothari, “Combination of melatonin and tamoxifen as a chemoprophylaxis against N-nitroso-N-methylurea-induced rat mammary tumors,” Cancer Letters, vol. 111, no. 1-2, pp. 59–66, 1997. View at Publisher · View at Google Scholar · View at Scopus
  172. S. Nowfar, S. R. Teplitzky, K. Melancon et al., “Tumor prevention by 9-cis-retinoic acid in the N-nitroso-N-methylurea model of mammary carcinogenesis is potentiated by the pineal hormone melatonin,” Breast Cancer Research and Treatment, vol. 72, no. 1, pp. 33–43, 2002. View at Publisher · View at Google Scholar · View at Scopus
  173. P. Kubatka, B. Bojková, M. Kassayová et al., “Combination of pitavastatin and melatonin shows partial antineoplastic effects in a rat breast carcinoma model,” Acta Histochemica, vol. 116, no. 8, pp. 1454–1461, 2014. View at Publisher · View at Google Scholar · View at Scopus
  174. R. T. Dauchy, S. Xiang, L. Mao et al., “Circadian and melatonin disruption by exposure to light at night drives intrinsic resistance to tamoxifen therapy in breast cancer,” Cancer Research, vol. 74, no. 15, pp. 4099–4110, 2014. View at Publisher · View at Google Scholar · View at Scopus
  175. L. G. de Almeida Chuffa, R. J. Reiter, and L. A. Lupi, “Melatonin as a promising agent to treat ovarian cancer: molecular mechanisms,” Carcinogenesis, vol. 38, no. 10, pp. 945–952, 2017. View at Publisher · View at Google Scholar · View at Scopus